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Top-down versus bottom-up forcing: Evidence


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Article in Journal of Mammalogy August 2012
DOI: 10.1644/12-mamm-a-014.1

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Top-down versus bottom-up forcing: evidence from mountain lions and mule deer
Author(s): Becky M. Pierce, Vernon C. Bleich, Kevin L. Monteith, and R. Terry Bowyer
Source: Journal of Mammalogy, 93(4):977-988. 2012.
Published By: American Society of Mammalogists
URL: http://www.bioone.org/doi/full/10.1644/12-MAMM-A-014.1

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Journal of Mammalogy, 93(4):977988, 2012

Top-down versus bottom-up forcing: evidence from mountain lions and


mule deer
BECKY M. PIERCE, VERNON C. BLEICH, KEVIN L. MONTEITH,*

AND

R. TERRY BOWYER

Department of Biological Sciences, 921 South 8th Avenue, Stop 8007, Idaho State University, Pocatello, ID 83209, USA
(BMP, VCB, KLM, RTB)
Sierra Nevada Bighorn Sheep Recovery Program, California Department of Fish and Game, 407 West Line Street,
Bishop, CA 93514, USA (BMP)
Wildlife Investigations Laboratory, California Department of Fish and Game, 1701 Nimbus Road, Rancho Cordova, CA
95670, USA (VCB)
* Correspondent: kmonteit@uwyo.edu
We studied mountain lions (Puma concolor) and mule deer (Odocoileus hemionus) inhabiting a Great Basin
ecosystem in Round Valley, California, to make inferences concerning predatorprey dynamics. Our purpose
was to evaluate the relative role of top-down and bottom-up forcing on mule deer in this multiple-predator,
multiple-prey system. We identified a period of decline (by 83%) of mule deer (19841990), and then a period of
slow but steady increase (19911998). For mule deer, bitterbrush (Purshia tridentata) in diets, per capita
availability of bitterbrush, kidney fat indexes, fetal rates (young per adult female), fetal weights, and survivorship
of adults and young indicated that the period of decline was typical of a deer population near or above the
carrying capacity (K) of its environment. Numbers of mountain lions also declined, but with a long time lag. The
period of increase was typified by deer displaying life-history characteristics of a population below K, yet the
finite rate of growth (k 1.10) remained below what would be expected for a population rebounding rapidly
toward K (k 1.151.21) in the absence of limiting factors. Life-history characteristics were consistent with the
mule deer population being regulated by bottom-up forcing through environmental effects on forage availability
relative to population density; however, predation, mostly by mountain lions, was likely additive during the
period of increase and thus, top-down forcing slowed but did not prevent population growth of mule deer. These
outcomes indicate that resource availability (bottom-up processes) has an ever-present effect on dynamics of
herbivore populations, but that the relationship can be altered by top-down effects. Indeed, top-down and
bottom-up forces can act on populations simultaneously and, thus, should not be viewed as a stark dichotomy.
Key words: density dependence, limitation, mountain lion, mule deer, nutrition, Odocoileus hemionus, predation, Puma
concolor, regulation, Sierra Nevada
2012 American Society of Mammalogists

DOI: 10.1644/12-MAMM-A-014.1

The concepts of top-down and bottom-up forcing are central


to the development of modern ecological theory (Hunter and
Price 1992; Power 1992; Strong 1992). These processes
influence trophic cascades (Berger et al. 2001; Terborgh et
al. 2001, 2006), ecosystem structure and function (McNaughton 1977; Molvar et al. 1993), biodiversity (Jacobs and Naiman
2008; Ripple and Beschta 2008; Stewart et al. 2009), and the
conservation of rare or endangered species (Aaltonen et al.
2009). Large mammalian herbivores and their predators are
important for studying top-down and bottom-up relationships
because theory developed from small animals may not apply to
large ones (Caughley and Krebs 1983; Sinclair and Krebs
2002).

Density-dependent mechanisms play an important role in


population dynamics of large herbivores (Boyce 1989; Kie et
al. 2003; McCullough 1979; Stewart et al. 2005). Diet quality
and niche dimensions vary with population density (Kie and
Bowyer 1999; Mobk et al. 2009; Nicholson et al. 2006;
Stewart et al. 2011), and life-history characteristics of large
herbivores are influenced strongly by density dependence
(Fowler 1981; McCullough 1999). The degree of resource
limitation (proximity to carrying capacity [K]) determines the

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JOURNAL OF MAMMALOGY

relative importance of top-down and bottom-up influences on


population dynamics (Bowyer et al. 2005; Kie et al. 2003). The
classic definition of K is when a population is at equilibrium
with its environment (Caughley 1977; McCullough 1979). We
extend that definition to include the long-term ability of a
particular environment to support viable populations of large
herbivores, wherein the population fluctuates around some
mean point of equilibrium. There may be, however, directional
changes in K as a result of long-term environmental change
(Kie et al. 2003).
There is considerable debate over the terms limitation and
regulation (Berryman 2004; White 2007); we argue that all
mortality factors are limiting, but only those resulting in a
density-dependent feedback are regulating. Herbivore populations near K are characterized by females attempting to produce
more young than can be recruited successfully into the
population (Bartmann et al. 1992; McCullough 1979), resulting
in mortality from predators that is primarily compensatory (i.e.,
the prey population remains near K)the population is limited
by predation, but regulated by density-dependent factors
associated with K. Conversely, in populations backed far away
from K, attempts to recruit young can be more successful if
predation was reduced because resources are not limiting; in
such situations mortality from predation tends to be additive
the population is not limited by resources, but is regulated by
predation. We contend that information on kill rates or
predation rates (Vucetich et al. 2011) are less meaningful than
data concerning the life-history characteristics of ungulates in
understanding predatorprey dynamics, because of the differences in the consequences of mortality as a function of the
proximity of the prey population to K.
The long-term investigations necessary to understand these
complex predatorprey relationships for large mammals are
uncommon, although several examples do exist (Jedrzejewska
and Jedrzejewski 2005; Vucetich et al. 2002). Nonetheless,
factors underpinning dynamics of large herbivores continue to
be debated, especially the role that large predators play in
affecting vital rates and demographics (Frank 2008; Terborgh
and Estes 2010; Terborgh et al. 2006). A lack of understanding
of the role of top-down forcing in ecological systems as a result
of the loss of large apex predators (Estes et al. 2011) and the
predator-centric focus of numerous predatorprey models
(Bowyer et al. 2005; Person et al. 2001) likely has hampered
our understanding of top-down and bottom-up processes for
these large mammals.
The theoretical development and debate over effects of topdown and bottom-up forcing on large herbivores largely began
with the world is green or Hairston, Smith, and Slobodkin
hypothesis (Hairston et al. 1960), which predicted that
herbivores were seldom limited by food and were, thus,
regulated by predation. In support of that hypothesis, cascading
effects of the absence of large predators are well documented
(Estes et al. 2011; Ripple and Beschta 2006, 2008; Terborgh
and Estes 2010; Terborgh et al. 2006), and in multiplepredator, multiple-prey systems, predation can regulate prey at
low densities relative to K (Bowyer et al. 1998; Dale et al.

1994; Gasaway et al. 1992; Van Ballenberghe and Ballard


1994). Nonetheless, the occurrence of predation does not
necessarily equate to top-down regulation; the degree of
predation and the interaction between the herbivore population
and its food supply determine the potential for top-down
regulation (Bartmann et al. 1992; Bowyer et al. 2005).
Assessing the relative strengths of top-down and bottom-up
forcing on regulation of populations, however, is of greater
theoretical value than debating which force is operating,
because both processes can occur simultaneously (Bowyer et
al. 2005; Boyce and Anderson 1999; Hunter and Price 1992).
We used a long-term data set on mountain lions (Puma
concolor) and mule deer (Odocoileus hemionus) that inhabited
a Great Basin ecosystem to evaluate the relative influences of
top-down and bottom-up forcing, because shifting dynamics of
this predatorprey system allowed for unique insights into the
role of large carnivores in regulating their ungulate prey. We
cast our predictions based on a conceptual model of life-history
characteristics for large herbivores proposed by Bowyer et al.
(2005; Table 1). In populations of mule deer regulated by topdown forcing, the population would be held far away from K,
mortality would be mostly additive, intraspecific competition
would be reduced, and individuals would have a morenutritious diet, resulting in better physical condition and, thus,
greater reproductive rates and higher survival. Conversely, in
populations regulated by bottom-up forcing, animals would be
at or near K, mortality would be largely compensatory,
intraspecific competition would be intensified, and a lessnutritious diet would lead to poor physical condition and,
thereby, lower reproductive rates and decreased survival (Table
1). In the absence of the aforementioned dichotomy, some
degree of nutritional limitation and effects of predation may cooccur, especially at intermediate densities in relation to K.

MATERIALS

AND

METHODS

Study area.Round Valley (37824 0 N, 118834 0 W), located


east of the Sierra Nevada in California, is the winter range for a
migratory population of mule deer, and the mountain lions that
prey upon them (Kucera 1992; Monteith et al. 2011; Pierce et
al. 1999). Mule deer inhabiting this Great Basin ecosystem are
the primary prey for mountain lions (Bleich et al. 2006; Pierce
et al. 2000b, 2004; Villepique et al. 2011). Annual precipitation
in the region was highly variable, and ranged from 5.3 to 25.2
cm. Precipitation was strongly seasonal, with about 72%
occurring during NovemberMarch, and mean monthly
temperatures ranged from 08C to 168C.
The predominant vegetation type in Round Valley is
sagebrush steppe (Pierce et al. 2004), and includes stands of
sagebrush (Artemisia tridentata), bitterbrush (Purshia tridentata), and rabbitbrush (Chrysothamnus nauseosus); patches of
blackbrush (Coleogyne ramosissima) and mormon tea (Ephedra nevadensis) also were common. Forbs, which were
generally unavailable to deer in winter, included Eriogonum
kennedyi and Lomatium sp. Common grasses were Stipa
speciosa, Oryzopsis hymenoides, Sitanion jubatum, Sitanion

August 2012

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PIERCE ET AL.TOP-DOWN VERSUS BOTTOM-UP FORCING

TABLE 1.Life-history characteristics, measures of physical condition, and vital rates of large herbivores, including predictions tested in this
study based on populations characterized by top-down forcing by large carnivores or bottom-up forcing through nutritional limitation (adapted
from Bowyer et al. [2005]).
Life-history characteristic
Physical condition of adult females
Pregnancy rate of adult females
Fetal rate
Weight of neonates
Mortality of young
Diet quality
Pause in annual production by adult females
Yearlings pregnant
Corpora lutea counts of adult females
Age at 1st reproduction for females
Age at extensive tooth wear

Top-down forcing

Bottom-up forcing

Predictions tested in this study

Better
Higher
Higher
Heavier
Additive
Higher
Less likely
Usually
Higher
Younger
Older

Poorer
Lower
Lower
Lighter
Compensatory
Lower
More likely
Seldom
Lower
Older
Younger

Yes
Yes
Yes
Yes
Yes
Yes
No
No
No
No
No

hystrix, and Bromus tectorum. Salix spp., Rosa spp., and Betula
occidentalis occurred in riparian areas (Kucera 1988).
Most mule deer inhabiting Round Valley during winter
migrated to high elevations (.2,500 m) on the west side of the
Sierra Nevada (Kucera 1992; Monteith et al. 2011; Pierce et al.
1999), where they used high-quality forage during summer
(Kucera 1997). Summer ranges were typified by high mountain
meadows associated with a variety of coniferous species
including Jeffrey (Pinus jeffreyi) and lodgepole (P. contorta)
pine. Deer remained on summer range until autumn, when
winter storms pushed them eastward over the Sierra crest and
downward to the valley floor (Monteith et al. 2011).
The population of mule deer overwintering in Round Valley
declined steadily from about 6,000 animals (66 deer/km2) in
1985 (Kucera 1988) to 939 (10 deer/km2) in 1991. Subsequently, the deer population rose to 2,165 (24 deer/km2) by
January 1999 (Fig. 1). The deer decline was associated with a
severe drought during 19871990, when water content of
winter snowpack was 27% of the long-term mean.

FIG. 1.Phases of population trajectory for mule deer (Odocoileus


hemionus) defined by piecewise regression, 19851999, and population trajectory for mountain lions (Puma concolor), 19931999,
during winter in Round Valley, California. Error bars for the deer
population from 1994 to 1999 are 95% confidence intervals. Adapted
from Bowyer et al. (2005).

In winter 1984, hunters killed 200 female mule deer (~3.3%


of the population) on the northern one-half of the study area
(Kucera 1988). Limited sport hunting for male mule deer
occurred during autumn in all years of our study. Hunting
opportunity on winter range in Round Valley resulted in the
harvest of approximately 15 males per year, but harvest of male
mule deer on summer range was difficult to estimate because
deer from Round Valley mingled with deer from other
populations. Nevertheless, limited harvest of males would
have had a negligible influence on population dynamics of deer
(Kie et al. 2003; McCullough 1979, 2001). No sport hunting of
mountain lions occurred during our study, and mountain lions
were killed only if they preyed on pets or livestock
(depredation), endangered Sierra Nevada bighorn sheep (Ovis
canadensis sierrae), or posed a threat to human safety (Torres
et al. 1996), a policy that had been in place for .1 decade prior
to the onset of our investigation.
Data collection.In many instances, we used results from
earlier investigations (Kucera 1988, 1991, 1997) combined
with our data to evaluate characteristics of this mule deer
population during a declining phase and the subsequent
increasing phase. We tested for differences in diets of deer
(percent of bitterbrush), per capita availability of bitterbrush,
physical condition (kidney fat index [KFI]), fetal rate (young
per adult female), fetal weight, survival of young, and survival
of adults during the periods of decline and increase of the deer
population. We also determined sources of mortality, and
estimated population sizes of mule deer and mountain lions.
We used microhistological analyses of fecal pellets (Sparks
and Malechek 1968) and digestibility of forages (Pierce et al.
2004) obtained monthly during winter to index percentage of
bitterbrush occurring in diets of mule deer from the northern (n
10 groups) and southern (n 10 groups) parts of the study
area. We collected only fresh (1-day-old) pellets, and
composited samples, by area, each month. Microhistological
identification of plant fragments was completed at the
Composition Analysis Laboratory, Fort Collins, Colorado.
Current annual growth (leader lengths) for bitterbrush was
sampled annually along 5 or 6 transects in autumn during most
years by personnel from the United States Bureau of Land
Management. Leader lengths were measured from 6 whorls

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JOURNAL OF MAMMALOGY

1.5 m above ground on 5 randomly selected plants along


each transect. All leaders of current year growth from each
whorl were measured until a minimum of 20 leaders on each
plant was measured.
We collected 20 female mule deer annually in March 1991
1995, following methods described by Kucera (1997). We
attempted to shoot only adult female deer, which were selected
at random throughout the study area and age, weight, body
condition, and fetal rate were recorded. Although we attempted
to collect only adult (2 years old) females, a few yearling
females were collected but differences in pregnancy and fetal
rates between adults and yearlings were accounted for in
subsequent analyses. We used 1 kidney from each deer to
determine physical condition with the KFI (Riney 1955). We
recorded weight of fetuses (6 1 g), but only of the heaviest if
.1 were present (Kucera 1988).
We used a helicopter and net gun (Krausman et al. 1985) to
capture mule deer (217 females and 93 males) in Round Valley
and fitted them with very-high-frequency radiocollars each
winter (~7% of the population) from 1993 to 1997. We
distributed collars among adult males and adult females in
proportion to their occurrence in the population (1:3). In
addition, we captured young (,1 year old; n 113) at random
and fitted them with expandable collars (Bleich and Pierce
1999). We intentionally avoided capturing deer from groups
that contained animals collared during previous years. We
monitored telemetered deer 6 or 7 times per week during winter
to determine survival and cause-specific mortality, and
monthly during summer to determine survival.
We conducted helicopter surveys each January to estimate
the proportion of adult male, adult female, and young (,1 year
old) mule deer on winter range, and obtain information on
population size. Aerial transects were flown with 3 observers,
and transects extended across the entire winter range to an
elevation at which deer tracks in snow were no longer evident.
In the early years (19841993), a total count of deer was
conducted (Kucera 1988) and no measures of variance could be
developed; nonetheless, the general trend of declining and
subsequently increasing deer numbers was unequivocal
(Bowyer et al. 2005). During 19941999, we used collared
animals to estimate the deer population and associated
variances (Chapman 1951); we used aerial telemetry 1 day
before each of these surveys to determine the number of
marked adult females within the survey area.
From 1994 to 1997, mule deer were evaluated for evidence
of diseases capable of causing a marked decline: brucellosis (n
538), infectious bovine rhinotracheitis (n 416), parainfluenza-3 (n 397), bluetongue (n 538), epizootic hemorrhagic
disease (n 538), leptospirosis (n 532), and anaplasmosis (n
535). Those data yielded no evidence of pathogens that could
have affected the population. Moreover, necropsy results (n
194 deer) during 19841996, yielded no evidence of any
ongoing disease.
During November 1991April 1999, we used hounds and
techniques described by Davis et al. (1996) to capture 21 adult
mountain lions (12 females and 9 males) in Round Valley and

Vol. 93, No. 4

fitted them with very-high-frequency radiocollars. We conducted regular and intensive searches for mountain lions
throughout the study area during 19911997, because these
large felids are capable of dispersing long distances (Thompson
and Jenks 2010). These intensive searches provided strong
evidence that all mountain lions that regularly used winter
range in Round Valley (i.e., resided for .30 days) were fitted
with radiocollars by 1993, and that immigrants were detected
and collared within 1 month of their arrival on winter range.
Detailed descriptions of searches for mountain lions and mule
deer killed by predators were provided previously (Pierce et al.
1998, 2000b, 2004).
We determined the mean number of collared mountain lions
on the study area during telemetry flights at weekly intervals
during NovemberMarch, and used that value to index the
number of adult mountain lions on winter range each year. We
excluded winter 19911992, because we captured the 1st
mountain lion during November 1991 and continued to capture
new, unmarked lions in Round Valley until November 1992,
by which time we had captured 12 adults. From then on our
ability to detect and capture new, unmarked lions was constant
from year to year (Pierce et al. 2000a, 2000b).
We also evaluated the number of depredation permits issued
for mountain lions to provide information on the annual
abundance of lions prior to 1992; number of permits issued,
however, does not represent the number of lions killed. We
assumed that depredation permits would be positively
associated with lion abundance, because additional conflicts
are expected as lion density increases (Torres et al. 1996). All
research methods were approved by an independent Animal
Care and Use Committee at the University of Alaska
Fairbanks, and complied with guidelines published by the
American Society of Mammalogists for research on wild
mammals (Sikes et al. 2011).
Analyses.We estimated number of deer born on summer
range by multiplying fetal rates in March by the estimated
number of adult females in the population. Survivorship of
young to 6 months-of-age was calculated from the number of
young estimated to have been born on summer range, and the
number of those young that arrived on the winter range, based
on composition counts conducted in early winter (Bleich et al.
2006). Survivorship of adult deer with radiocollars was
calculated with the KaplanMeier estimator (Pollock et al.
1989) and proportions of cause-specific mortality during winter
were determined according to Heisey and Fuller (1985).
We used piecewise regression (Neter et al. 1990) to define
periods of population change, although an estimate for the
population was not available for 1990; thus, we used regression
analysis to estimate the value for 1990 for use in subsequent
analyses. We calculated the finite rate of population growth (k)
as the inverse log of the slope of the regression on the natural
log of population size through time (Caughley 1977). We used
analysis of covariance (Neter et al. 1990), with Julian date of
collections as a covariate to adjust weight of fetuses among
years for dates of collection. We developed a densitydependent index to the availability of bitterbrush as an

August 2012

PIERCE ET AL.TOP-DOWN VERSUS BOTTOM-UP FORCING

indication of forage available to deer (mean leader-length per


deer in the population during winter 3 100); this index is
influenced by changes in the number of bitterbrush leaders over
time in relation to the density of the deer population.
We tested for effects of weather on forage availability and
condition of mule deer, as well as the relationships between
deer diet, body condition, reproduction, and k using the
Spearman rank correlation (rsConover 1980). We also used
rs to test for the relationship between survivorship of young on
summer range and k for all years pooled, and for the same
comparisons during periods of decline and increase in the deer
population. Spearman rank correlations make no assumptions
about the shape of relationships between variables (Conover
1980); thus, figures include lines of best fit only as an aid to
interpret those relationships.
We used the MannWhitney U-test (Conover 1980) to
examine differences in mean temperatures during December
February, leader length of bitterbrush, the index to the
availability of bitterbrush, percent bitterbrush in diets, KFI,
fetal rates, fetal weights, and survivorship of young and adult
mule deer between periods of decline and increase of the deer
population. We maintained an a 0.05 for those comparisons,
except analyses where KFI, fetal rate, and fetal weight were
obtained from the same individual; for those tests, we corrected
experiment-wide error with a sequential Bonferroni procedure
(Rice 1989). We also used this correction for correlations
between weather variables and life-history characteristics of
deer. We used rs to compare the number of depredation permits
issued with our index to lion abundance from 1993 to 1999,
and subsequently to evaluate the relationship between deer
abundance and number of depredation permits issued during
both phases of population change.
We used a life table with 3 age classes (0, 1, and 212 years
of age) and sexes combined to estimate adult survivorship each
year. We did not calculate survivorship of deer directly because
those data were available for only 4 years; for consistency, we
used the life-table analysis to calculate survivorship for the
entire study period. We used fetal rates corrected for the entire
population, survivorship of young on summer range, and the k
estimated for each year in the life-table analyses. We assumed
survivorship for yearlings and adults to be similar, and
survivorship was adjusted until a k matching the observed
value for a particular year was obtained. Violation of this
assumption would have had negligible effects on resulting
survival rates for adults because yearlings comprised a small
component of the population relative to adults. For yearlings,
fetal rates during the period of decline were set at 0; we used
fetal rates of 0 during 19911993, and of 1 during 19941996,
based on data from deer collections.
Life tables assume a stable age distribution, and can
overestimate the importance of adult survivorship when k is
fixed (Bowyer et al. 1999; Caughley 1977; Eberhardt 1985);
however, calculating parameters repeatedly on an annual basis
minimized that potential bias. Moreover, we did not use that
analysis to determine the relative role of adult survivorship on
population growth, but only to compare survivorship between

981

2 periods for which it was estimated in the same manner. Thus,


any upward bias in the importance of adult survivorship should
not have affected our results markedly.
Testing predictions for whether top-down or bottom-up
forcing occurred in this population of mule deer involved a
variety of statistical procedures, all of which were directed at a
similar hypothesis (Table 1). Consequently, we combined
probabilities from those statistical tests using the method of
Sokal and Rohlf (1981):
X
lnP;
v2 2
with 2k degrees of freedom, where k is the number of separate
tests. We recognize that our tests were not completely
independent; accordingly, we reduced alpha for this analysis
to 0.02 (Bowyer et al. 2007). Meta-analyses using this
approach have been increasingly recognized as valuable tools
in ecology when probabilities used in the analyses are focused
on single hypotheses (Arnqvist and Wooster 1995; Osenberg et
al. 1999).

RESULTS
Predation and population trajectory.Piecewise regression
identified 2 trajectories of population size for mule deer: a
declining phase (19841990) and an increasing phase (1991
1998; Fig. 1). The k of the deer herd in Round Valley during
the drought of the late 1980s reflected a marked decline (r2
0.98, P , 0.001) followed by a phase of slow population
growth (r2 0.82, P , 0.001) in the 1990s (Fig. 1).
Mean number of adult mountain lions inhabiting Round
Valley during winter declined from 6.1 in winter 19921993 to
0.6 in winter 19981999 (r2 0.95, P , 0.001; Fig. 1). During
that period, we documented 20 mortalities of radiocollared
lions: 10 males and 10 females. Sources of mortality included
malnutrition (n 3), killed because of depredation on domestic
sheep or Sierra Nevada bighorn sheep (n 6), intraspecific
strife (n 2), illegal killing (n 3), vehicle collision (n 1),
and causes that could not be determined (n 5). Of the 6
mountain lions killed on depredation permits, 3 were in poor
physical condition. The population of mountain lions tracked
mule deer numbers downward, but with a time lag of about 8
years (based on data from 1992 to 1999; Fig. 1). In addition,
the number of depredation permits was strongly correlated with
lion abundance from 1993 to 1999 (rs 0.81, P 0.027); this
outcome substantiated the annual number of depredation
permits as an index to the abundance of mountain lions.
Despite the directional change in the trajectory of the deer
population in 1991 (Fig. 1), and with the exception of an
outlier in 1985, depredation permits issued for mountain lions
declined from 1986 to 1999 (Fig. 2). Prior to 1985, when the
deer population was probably high or increasing, few annual
permits for lion depredation from 1972 to 1984 were issued (X
1.3, SE 0.44). During the declining phase of the deer
population, lion abundance was not related to deer numbers (rs
0.29, P 0.27), even though substantially more permits for
lion depredation were issued annually (X 11.6, SE 1.03).

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JOURNAL OF MAMMALOGY

The increased killing of mountain lions had no discernible


effect on the continued decline of mule deer through 1990 (Fig.
2), a pattern contrary to expectations if top-down forcing
occurred. Following the crash of the deer population, number
of depredation permits issued continued to decline (X 7.6, SE
1.44), with the exception of 1996 when an abnormally high
number of permits was issued (Fig. 2). Nevertheless, number of
depredation permits issued was negatively related to deer
abundance (rs 0.63, P 0.069). Predation by mountain
lions was the most significant cause of mortality for mule deer
in all years (Fig. 3) except 1998, when predation by coyotes
(Canis latrans) surpassed that of mountain lions.
Diet, animal condition, reproduction, and survival.Per
capita availability of bitterbrush and the percent of bitterbrush
in diets of mule deer were significantly greater during the
period of population increase than during the period of decline
(Table 2). We identified a strong relationship between leader
length of bitterbrush and total water content of snowpack
measured in April (Fig. 4). That relationship was positive
during the period of decline (rs 0.83, P 0.010), and waned
during the period of increase (rs 0.43, P 0.29). A strong
positive relationship also existed between per capita
availability of bitterbrush and body condition of deer (as
indexed by KFI) during the declining phase (rs 1.0, P ,
0.001); this relationship weakened during the increasing phase
(rs 0.2, P 0.74). As percent bitterbrush in the diet in March
increased from 2% to 10%, physical condition (as indexed by
KFI) of mule deer rose exponentially and became asymptotic
when bitterbrush in diet was .30% (Fig. 5). Mean winter
temperature also was positively related to KFI, but not
significantly so following a Bonferroni correction (rs 0.62,
P 0.05), and did not differ between periods of population
decline and increase (U11 33.0, P 0.9).

FIG. 2.Phases of population trajectory for mule deer (Odocoileus


hemionus) and the number of mountain lion (Puma concolor)
depredation permits issued in Inyo and Mono counties, 19851999,
Round Valley, California. Error bars for the deer population from
1994 to 1999 are 95% confidence intervals. Depredation permits were
positively correlated with number of lions present in Round Valley
and, hence, provided a viable index to mountain lion abundance.

Vol. 93, No. 4

FIG. 3.Cause-specific mortality (n 115) of mule deer


(Odocoileus hemionus) during winter in Round Valley, California,
during the increasing phase, 19931998 (error bars are 95%
confidence intervals).

Fetal rates were 13% lower during the period of population


decline than when the population was increasing (Table 2).
Following a Bonferroni correction, fetal rates were related
positively to KFI of female mule deer, which was significant
during the increasing phase (rs 0.94, P 0.005) but not
during the decline (rs 0.83, P 0.05). Mean weight of fetuses
adjusted for age also was 14% less during the period of decline
than during the period of increase (Table 2). The relationship
between KFI and fetal weight was not significant during the
decline (rs 0.20, P 0.8), but was strongly negative during
the period of increase (rs 0.89, P , 0.001). That negative
relationship, however, more likely was driven by the higher
fetal rate during the period of population increase (rs 0.94,
P , 0.001) than during the decline (rs 0.52, P 0.2; Table
2).
Mean annual survivorship of adults differed significantly and
was 24% lower during the period of decline than the period of
increase (Table 2). Reduced survivorship among adult females
was likely the underlying demographic cause of the population
crash from 1985 to 1990. In contrast, survivorship of young on
summer range was statistically similar between periods of
decline and increase (Table 2). Following Bonferroni corrections, meta-analysis indicated that characteristics of mule deer
differed during periods of population increase and decline (v214
38.8, P , 0.001).
Finite rate of increase (k).When population trajectories of
mule deer were considered separately, in all instances, k was
,1.0 when the mean percent of bitterbrush in diets of mule
deer in March was 10%. Although KFI of mule deer was
positively correlated with k, that relationship was not
significant (rs 0.31, P 0.36). No significant relationship
(rs 0.32, P 0.38) existed between winter temperature and k
for the deer population across years. A significant relationship

August 2012

983

PIERCE ET AL.TOP-DOWN VERSUS BOTTOM-UP FORCING

TABLE 2.Population characteristics of a wintering population of mule deer (Odocoileus hemionus) in Round Valley, California, during
decreasing and increasing trajectories of population size. P-values are results of MannWhitney U-tests for differences in characteristics of the
population between decreasing and increasing phases. Results from the declining phase are from Kucera (1988). All P-values  0.02 are
significant following a Bonferroni correction.
Declining phase (19841990)

Increasing phase (19911998)

Population characteristic

SE

Range

SE

Range

P-value

Bitterbrush in deer diets (%)


Per capita availability of bitterbrush (cm/deer 3 100)
Kidney fat index
Fetal rate (young/adult)
Fetal weight (g)a
Survivorship of young
Survivorship of adults

5.40
0.13
28.00
1.40
156.70
0.22
0.65

1.10
0.05
8.70
0.08
13.10
0.01
0.03

2.510.0
0.010.34
12.068.0
1.21.72
116.3202.2
0.160.25
0.590.73

43.40
0.56
33.30
1.60
182.10
0.26
0.86

13.20
0.12
7.70
0.08
18.60
0.03
0.04

7.378.9
0.121.24
10.456.0
1.41.8
126.1258.8
0.160.38
0.691.0

0.006
0.007
0.750
0.100
0.260
0.390
0.012

Weight was adjusted by Julian day of collection.

between k and survival of young during the period of decrease


(rs 0.90, P 0.04) did exist, but not when the population was
increasing (rs 0.21, P 0.65).

DISCUSSION
Our approach was to evaluate the relative role of top-down
and bottom-up forcing in a mule deer population using a
conceptual model (Bowyer et al. 2005; Table 1) based on the
life-history characteristics of ungulates (Eberhardt 1985;
Gaillard et al. 2000) linked with their nutritional condition
(Parker et al. 2009) to parameterize deer population characteristics in relation to K. The conceptual model was developed in
reference to directional changes in important life-history
characteristics that are expected under top-down or bottomup regulation, but does not necessarily make assumptions
about the magnitude of change for a particular variable. The
significance of a single variable in this interpretation is less

FIG. 4.Length of annual growth of bitterbrush leaders (important


winter forage for mule deer [Odocoileus hemionus]) in relation to
water content of snowpack measured in April during the declining
phase (19851990) and increasing phase (19911998) of the
population of mule deer in Round Valley, California.

important than the overall pattern and direction of an influential


set of life-history characteristics. Therefore, we used a weightof-evidence approach (sensu Bowyer et al. 2003), wherein
information from a single variable is insufficient to draw
conclusions, but when multiple variables are considered in
concert, a strong and clear pattern may emerge.
Although some of the individual population characteristics
in Table 2 did not differ between periods of decline and
increase, all differences were in the predicted direction based
on the physical condition of deer. Characteristics were
consistent with bottom-up forcing regulating the population
of mule deer through environmental effects on forage
availability relative to population density; however, top-down
forcing (i.e., predation) had a modest, but negative effect (a
reduction of 511% per annum) on population growth while
the population was recovering from the crash (Fig. 1; Table 2).
These outcomes align with the premise that variation in

FIG. 5.Percent bitterbrush in diet of mule deer (Odocoileus


hemionus) during March in relation to mean kidney fat index of
female mule deer collected in March during the declining phase
(19851990) and increasing phase (19911998) of the population of
mule deer in Round Valley, California. Results from the decreasing
phase are from Kucera (1988).

984

JOURNAL OF MAMMALOGY

resource availability (bottom-up) permeates through the system


and has an ever-present effect, which may be altered by topdown effects (Hunter and Price 1992). Indeed, top-down and
bottom-up forces can act on populations simultaneously and,
thus, should not be viewed as a stark dichotomy (Bowyer et al.
2005; Boyce and Anderson 1999), an outcome that is
inconsistent with expectations of the Hairston, Smith, and
Slobodkin hypothesis.
Our results illustrate the importance of obtaining long-term
information on the physical condition and vital rates of the prey
population, which also has been emphasized by others
(Barboza et al. 2009; Bishop et al. 2009; Parker et al. 2009).
Considering only the size or density of the population of mule
deer (and in later years the number of mountain lions) would
have supported a conclusion that mountain lions regulated
mule deer in the declining phase and failed to do so during the
increasing phase (Figs. 1 and 2)a supposition contradictory
to our conclusions. Studies assessing the degree of top-down
and bottom-up forcing typically have not included data on
physical condition of prey, an omission that may cloud
interpretation of results. Furthermore, a less lengthy investigation might have concluded that forcing was either from below
or above, depending on the phase of the population trajectory
sampled (Fig. 1).
The population decline of mule deer probably was not the
result of severe winter weather in this Great Basin ecosystem;
we documented only positive effects of snowpack on mule deer
via increased forage growth (Fig. 4) that, in turn, resulted in
improved physical condition. During the period of increase, we
observed limited effects of snowpack on forage consumption
or k, likely because deer were released from severe nutritional
limitation (Table 2). Bitterbrush in diets of deer was positively
correlated with the KFI during the decline, but not when the
deer population was increasing. Consequently, density-independent factors (e.g., severe weather) likely were not
responsible for the population decline via effects on the energy
budget of deer, and were unrelated to population characteristics
during the period of increase. Moreover, no evidence existed
that diseases were responsible for the decline in numbers of
mule deer, or for slowing their rate of recovery.
If predation was an additive source of mortality during the
decline, the condition of deer should not have been strongly
correlated with their food supply (Bowyer et al. 2005; Kie et al.
2003; McCullough 1979). Indeed, we would not have expected
mortality to be additive (i.e., top-down forcing) when levels of
bitterbrush in diets of deer were low (,10%), deer were in
comparatively poor physical condition, and reproductive rates
were lowall characteristic of a declining and nutritionally
regulated population. Primarily top-down forcing should have
resulted in deer being in good physical condition, because they
would have been better buffered against, and less influenced
by, slight fluctuations in their food supply, particularly during
the period of decline. Bitterbrush in diets of deer, per capita
availability of bitterbrush, KFIs, fetal rates, fetal weights,
survivorship of young, and survivorship of adult females all
were lower during the period of decline than the period of

Vol. 93, No. 4

increase for mule deer (Table 2). These results clearly indicate
that mule deer in Round Valley were at or near K of the winter
rangeconditions that precipitated the population decline
and that mortality during that time, regardless of the proximal
cause, was largely compensatory.
The prolonged drought during the period of decline likely
lowered K for mule deer. This deer population, however, was
in decline before the start of the drought, which commenced in
1987 (Fig. 1). Similarly, McCullough (2001) demonstrated that
strong density-dependent processes continued to operate for a
population of deer during the course of a 6-year drought.
Although we cannot determine conclusively what caused the
initial crash in mule deer numbers, an overshoot of K followed
by a severe drought is a plausible explanation. Populations of
large herbivores exhibit strong density dependence (Kie et al.
2003; McCullough 1999; Stewart et al. 2005), and population
irruptions with overshoots of K are well documented (Forsyth
and Caley 2006; Klein 1968; McCullough 1979).
Several lines of reasoning indicate that top-down forcing
was operating during the period when mule deer numbers were
increasing. Although a proximal cause of mortality is
insufficient evidence to interpret the consequences of mortality
(Bartmann et al. 1992; Bleich et al. 2006), mountain lions were
the primary source of winter mortality for mule deer during the
increase (Fig. 3). We obtained little evidence that food was
limiting during the period of increasing numbers of mule deer
(Table 2). Indirect effects of predation risk (Berger 2010) were
likely minimal because deer selected habitat that simultaneously reduced predation risk and enhanced forage benefits (Pierce
et al. 2004). Christianson and Creel (2010) reported a similar
situation for North American elk (Cervus elaphus) preyed upon
by gray wolves (Canis lupus). Moreover, the stress and
associated physiological responses to predation risk should
have been strongest after the population crash when mountain
lion abundance lagged behind the deer population (Creel et al.
2007). In contrast to that presumption, fetal rates and
nutritional status were greater during the period of increase
than during the declining phase (Table 1).
In June 1995, a fire burned 22 km2 (24%) of the winter range
dominated by sagebrush and bitterbrush. The loss of winter
habitat associated with the fire in 1995 did not markedly affect
variables associated with the physical condition or life-history
characteristics of mule deer, because the deer population was
relatively low (Fig. 1) and forage availability remained high
(Table 2). Therefore, predation by mountain lions likely was an
additive source of mortality during the period of increase.
Moreover, k for mule deer was only 1.10 during the increase,
whereas mule deer can attain k 1.151.21 when not limited
by food or predation (Kie and Czech 2000). Top-down forcing
by mountain lions and other carnivores likely slowed, but did
not prevent, recovery of mule deer in this Great Basin
ecosystem. Whether the deer population ultimately will return
to the 6,000 animals present on the winter range in the 1980s,
and how changes in available resources will alter K, is a topic
for future research.

August 2012

PIERCE ET AL.TOP-DOWN VERSUS BOTTOM-UP FORCING

We encountered several challenges while conducting our


research. We combined our results with those reported by
Kucera (1988, 1991, 1997) to obtain a sufficient number of years
to encompass the trajectories of this population of mule deer. As
a result, we often had access to only mean values with no
associated measures of variance, which necessitated the use of
nonparametric statistics for most analyses. Our approach also
required that we duplicate the methods of Kucera (1988) as
closely as possible to allow meaningful comparisons. These
methodologies led to some inconsistencies in our results. For
example, KFI is less sensitive to changes in physical condition
when cervids have high fat reserves (Cook et al. 2007), which
explains why KFI exhibited a curvilinear pattern with increasing
bitterbrush in diets (Fig. 5) and did not differ markedly between
periods of differing population trajectories (Table 2).
Sampling only the largest fetus may have caused us to
underestimate the total weight of fetuses from females with
twins. Fetal rates were higher during the period of increase than
decline and, consequently, twins were more plentiful (Table 2).
Singletons often weigh more than individuals from a set of
twins (Kucera 1991), which likely introduced a bias into our
data; total fetal weight might have produced a greater
difference between phases of population decline and increase.
Another factor reducing the difference in fetal weights and
associated survivorship of young between periods of population decline and increase could be a residual maternal effect
(Monteith et al. 2009). Indeed, survivorship of young increased
only slightly during the increasing phase (Table 2). Intergenerational maternal effects caused by severe nutritional
limitation during the decline may have resulted in lags in
population response, and thereby have the potential to mask
expected patterns related to top-down or bottom-up forcing
from the body size of animals (Monteith et al. 2009).
Grange and Duncan (2006) reported that populations of
plains zebras (Equus quagga) were more resistant to drought
than were populations of other grazing ruminants such as blue
wildebeest (Connochaetes taurinus) and buffalo (Syncerus
caffer). Those authors concluded that zebras were more likely
to be influenced by top-down forcing by African lions
(Panthera leo), whereas populations of wildebeest and buffalo
were limited principally by their food supply. Moreover,
Wilmers et al. (2007) concluded that stalking predators, such as
mountain lions, were more effective at suppressing fluctuations
in their prey than were cursorial hunters, such as wolves and
coyotes. Even an effective stalking predator such as the
mountain lion (Knopff et al. 2010; Pierce et al. 2000a, 2000b),
however, only slowed the recovery of the mule deer population
in Round Valley. The resistance of the prey population to food
shortages, and the type of predator and its hunting style, hold
potential to influence the magnitude of bottom-up and topdown forcing.
Our results demonstrate that top-down forcing from multiple
predators may limit population growth but does not always
regulate prey populations. Mountain lions and other large
carnivores in our study area slowed, but did not regulate, the
growth of a mule deer population. More attention needs to be

985

given to the specific conditions that lead to equilibria or


disequilibria between populations of large mammalian predators and their prey (Hunter and Price 1992), and whether those
factors lead to population irruptions and overshoots of K with
subsequent effects on ecosystem structure and function. This
approach is likely to be critically important for the conservation
of large mammals in a changing climate, where directional
changes or dramatic variation in K may become the norm.

ACKNOWLEDGMENTS
We thank the houndsmen and others who helped capture mountain
lions and locate mule deer killed by mountain lions, including W. J.
Allsup, C. S. Baker, C.-L. Chetkiewicz, J. L. Davis, R. A. Noles, J. W.
Ostergard, P. E. Partridge, G. Raygorodetsky, D. C. Stoner, and J. D.
Wehausen. This research was supported by the California Department
of Fish and Game, University of California White Mountain Research
Station, the Department of Biological Sciences at Idaho State
University, National Rifle Association, Friends of the National Rifle
Association, Mule Deer Foundation, Safari Club International (Los
Angeles, Orange County, Sacramento, San Fernando Valley, and San
Francisco Bay Area chapters), Fish and Game Advisory Committee of
Inyo and Mono counties, and the Institute of Arctic Biology at the
University of Alaska Fairbanks. We thank K. M. Stewart, R. A. Long,
J. C. Whiting, J. L. Rachlow, W. P. Smith, and 2 anonymous
reviewers for their helpful comments on our manuscript. This is
Professional Paper 085 from the Eastern Sierra Center for Applied
Population Ecology.

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Vol. 93, No. 4

WILMERS, C. C., E. POST, AND A. HASTINGS. 2007. The anatomy of


predatorprey dynamics in a changing climate. Journal of Animal
Ecology 76:10371044.

Submitted 19 January 2012. Accepted 11 February 2012.


Associate Editor was Winston P. Smith.